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Articles in PresS. J Appl Physiol (May 4, 2006). doi:10.1152/japplphysiol.01380.2005
Mechanisms for the control of respiratory evaporative heat loss in panting
animals
David Robertshaw,
Weill Cornell Medical College in Qatar,
Running Head: “Control of Panting”
Address for correspondence:
David Robertshaw
Weill Cornell Medical College in Qatar,
P O Box 24144, Doha, Qatar.
Email: <[email protected]>
Tel no.: (974) 4928 201
Fax no: (974) 4928 222
Copyright © 2006 by the American Physiological Society.
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Control of Panting
Abstract
Panting is a controlled increase in respiratory frequency accompanied by a decrease in
tidal volume the purpose of which is to increase ventilation of the upper respiratory tract,
preserve alveolar ventilation, and thereby elevate evaporative heat loss. The increased energy
cost of panting is offset by reducing the metabolism of non-respiratory muscles. The panting
mechanism tends to be important in smaller mammalian species and in larger species is
supplemented by sweating. At elevated respiratory frequencies and body temperatures alveolar
hyperventilation begins to develop but is accompanied by a decline in the control of carbon
dioxide partial pressure in arterial blood probably through central chemoreceptors. Most heat
exchange takes place at the nasal epithelial lining and venous drainage can be directed to a
special network of arteries at the base of the brain whereby counter-current heat transfer can
occur which results in selective brain cooling. Such a phenomenon has also been suggested in
non-panting species including man and although originally thought to be a mechanism for
protecting the thermally vulnerable brain is now considered to be one of the thermoregulatory
reflexes whereby respiratory evaporation can be closely controlled in the interests of thermal
homeostasis.
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Introduction
Loss of heat by utilisation of the latent heat of vaporization of water is an important
component of the spectrum of physiological strategies available to species that control their
body temperature in the face of variable thermal loads. The best methods known of increasing
evaporative heat loss are panting, sweating and saliva spreading. This review will focus on
panting as a thermolytic strategy. A lot of the research into panting occurred before 1975 with
a revival of interest after 1995 that accompanied technical advances in both telemetry and data
collection and analysis.
Respiratory Evaporation:
The function of the respiratory system is often viewed as being related primarily to gas
exchange, and other functions such as acid base control, phonation and thermoregulation are
often overlooked. The evolution and success of endothermy allowed the control of body
temperature in cold environments to be independent of the external thermal environment but
required the development of appropriate heat loss strategies in hot environments.
Since
respiratory gas exchange requires the humidification of inspired air, an increase in respiratory
ventilation will also elevate respiratory evaporation as long as respiratory dehumidification and
cooling does not occur (35). Thus, evaporative heat loss by panting would be a relatively
simple function to accommodate. In terms of evaporative heat loss of terrestrial endotherms it
is possible that, from an evolutionary standpoint, either panting or saliva spreading may have
been the first heat loss mechanisms to emerge that utilized the latent heat of vaporization of
water to increase heat loss. However, alveolar exchange of oxygen and carbon dioxide would
also need to be controlled in order to preserve the requirements for gas exchange and pH
homeostasis. Ideally the increase in ventilation should be confined therefore to the dead space
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where humidification takes place and should not compromise alveolar gas exchange, a
requirement which can be achieved by an increase in respiratory frequency with a
proportionate decrease in tidal volume (15) which, in fact, becomes a definition of panting
(Figure 1). If one reviews the extent to which panting is used as an evaporative heat loss
mechanism in the animal kingdom it is found to occur in some reptiles, in birds and in many
mammalian species. There is a difficulty in determining from visual measurement of
respiratory frequency alone that panting, as defined, truly exists. Only the technically difficult
approach used in Figure 1 whereby respiratory ventilation is partitioned into its alveolar and
dead space components or direct measurement of respiratory water loss will truly satisfy the
conclusion that panting is an evaporative heat loss mechanism.
However careful visual
observation as to the changes in the depth of respiration will often discriminate between
increases associated with panting, exercise or the hypermetabolism of hyperthermia.
The most notable non-panting species in mammalian terrestrial species (marine
mammals for obvious reasons relating to the physics of heat transfer in water need no such
mechanism) are the elephant and man. The elephant has no identified evaporative heat loss
mechanisms that can be activated as part of thermal homeostasis; the elephant simply stores
heat during the day and dissipates it at night (16). Primates, other than man, demonstrate
panting to a limited extent (17). In man no respiratory response to heat exposure falls within
the definition of panting.
When a comparison is made of the relative efficacy of the two main modes of
evaporative heat loss, i.e. panting and sweating, it is often concluded that, although the
movement of air across the moist surfaces of the turbinate bones in the nasal cavity assists in
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the evaporation of water in a way not generally available to the skin surface of sweating
species, the heat loss of panting is limited by the increase in heat production of the muscles of
respiration. However, the energy cost of panting, when measured as the change in total oxygen
consumption between the thermoneutral and thermolytic zones is found to be zero (12, 14);
truly an efficiency of 100%! The solution to this paradox was revealed by Hales (11) who
compared the distribution of cardiac output before and during heat exposure and demonstrated
that an increase in blood flow to the respiratory muscles during panting was compensated by a
reduction in flow to some of the non-respiratory muscles leading to the conclusion that, if
blood flow and oxygen consumption are matched, the metabolism of respiratory muscle may
indeed be elevated during panting but that of other muscles would be equally depressed. An
additional feature which contributes to the high energetic efficiency of panting is that the
maximum panting frequency occurs at the resonant frequency of the respiratory system (5).
Since the maximal panting frequency will therefore be inversely related to body size this may
explain the observation that in a range of bovid animals of different adult body size that use
both panting and sweating, the larger species utilize sweating more than panting as a strategy
for increasing evaporative heat loss (33). One may speculate, therefore, that if panting
represents a primitive form of evaporative heat loss of the early mammals, which were small,
the subsequent evolution of larger species necessitated the development of a supplementary
form of evaporative heat loss, namely sweating. Evaporative heat loss of the kangaroo is
unique in that all three strategies for increasing evaporation are used; saliva spreading and
panting at rest and sweating during exercise (7).
Thermolysis and gas exchange
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The water and heat loss of respiration is dependent on both ambient humidity and
minute ventilation. Under cold conditions, both convective and evaporative respiratory heat
loss is largely uncontrolled and may need to be countered by an elevation of both metabolism
and respiratory ventilation in the interests of thermal homeostasis. Thus high altitude
mountaineers in a hypoxic environment with an increased respiratory ventilation and inhaling
air of low humidity are faced with the dual threats of significant water and heat loss which may
contribute to the risk of both dehydration and hypothermia. However, a reduction in minute
ventilation upon exposure to cold temperatures will lead to hypercapnia and increased oxygen
extraction from inspired air (37). A detailed study on the effects of cold exposure on the
respiration of cattle demonstrated a reduction in total respiratory heat loss, expressed as a
percentage of metabolic heat production, which was inversely proportional to ambient
temperature and accompanied by arterial hypercapnia and hypoxemia (8). The respiratory
system can be seen therefore to be responsive to, and be part of, a cascade of reactions to the
thermal environment with a continuum extending from hypoventilation in the cold to
hyperventilation in the heat.
Although the increase in ventilation in panting are largely confined to the dead space
there is inevitably a small but detectable increase in alveolar ventilation and a consequent
hypocapnia; dead space ventilation cannot be physically separated from alveolar ventilation
and diffusive mixing of gases is bound to occur. If evaporative heat loss is inadequate and
body temperature rises there is a change in the pattern of respiration such that tidal volume
increases and respiratory frequency decreases and panting changes from closed to open mouth
respiration. The consequent alveolar hyperventilation leads to a progressive development of
profound respiratory alkalosis (15). Thus two forms of panting have been described; one,
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without any major change in alveolar ventilation and the other initiated as core temperature
rises in which there is significant alveolar hyperventilation. (Figure 1). One explanation for the
hyperthermic hyperventilation might be that the resistance to nasal airflow increases to such an
extent that a change to a low resistance mode of ventilation i.e., through the mouth, would
become necessary. The elegant model of respiratory air flow based on anatomical
measurements of the turbinates devised by Schroter and Watkins in 1989 (36) indicates that the
Reynolds number in the gaps are low enough to predict that even at high ventilation rates air
flow will always be laminar and airway resistance is unlikely to be a factor in the transfer to
open mouth panting.
Exercise can lead to hyperventilation in many species and the question has been posed
that in addition to the anticipatory hyperventilation that occurs in humans before exercise the
respiratory stimulus(i) for hyperventilation may be multifactorial originating from exercising
muscles themselves and thus be a function of exercise intensity, or from a rise in blood lactate
concentration or be part of the thermoregulatory drive. In studies conducted on sheep, which is
a panting species, Entin et al in 1998 (10) identified body temperature as the only significant
variable in exercise-induced hyperventilation. In both passive or exercise-hypernea,
thermoregulatory drive appears to be the common modality. However, the hyperthermic
hypocapnia may suppress the chemoreceptor drive to respiration. This apparent conflict has
been examined in three studies. Hales et al (13) denervated the carotid chemoreceptors and
found no evidence of any significant role for the peripheral chemoreceptors in the ventilatory
response to heating in sheep. Maskrey et al (28) enriched the inspired air of sheep with carbon
dioxide to maintain normocapnia and found a reduction in panting frequency and an increase in
tidal volume which suggested that the threshold chemoreceptor response to carbon dioxide was
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lowered by hyperthermia. Entin et al (9) also concluded that as body temperature rises there is
a downward shift in the control level or “set point” of arterial pCO2 which offsets any apparent
homeostatic conflict between thermolysis and pH control. Such an adjustment of either
respiratory threshold or sensitivity to pCO2 may be significant in species that rely on panting
as their main means of evaporative heat loss in that it removes any possible “braking” effect of
hypocapnia on thermolysis.
Studies on Man
If it is accepted that there is little or no evidence for panting as a thermoregulatory
mechanism in man then the effects of either passive or exercise-induced hyperthermia on
respiration should separate the uniquely respiratory consequences of hyperthermia from those
related to temperature regulation. The work of Cabanac & White (4) and White & Cabanac
(39) showed that, contrary to the situation in panting species where there is no clear threshold
body temperature for the onset of hyperventilation (10), a change in respiration occurs only
when core body temperature has risen to a threshold value; once a threshold temperature is
exceeded hyperventilation ensues. This threshold is significantly higher than the threshold
temperatures for both the onset of sweating and increase in cutaneous blood flow
demonstrating that the respiratory response to hyperthermia cannot be analogous to the panting
response and be part of the usual group of thermolytic reflexes (38). The hyperthermic
hyperventilation observed in panting species, such as dog and sheep, may be analogous
therefore to that observed in non-panting man and therefore be a fundamental property of the
respiratory system of all species of bird and mammal whether or not they use panting as a heat
loss mechanism. The feature which is common to man and non-panting animals could be the
relationship between respiration and selective brain cooling.
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Selective Brain Cooling
Panting involves inhalation of air through the nose and in most species the mouth is
closed. Although it is common knowledge that the dog shows open mouth panting inspired air
enters the nasal cavity and exits through the mouth (34). Humidification of the inspired air
therefore occurs from fluid secreted on to the surface of the nasal epithelium (3). An increase
in blood flow to the nasal mucosa provides the necessary heat for evaporation and the venous
blood draining the turbinates is thereby cooled. The subsequent distribution of the venous
blood is variable; it may enter either the angularis occuli vein and then to the cranial cavernous
sinuses before finally entering the jugular vein or alternatively it may enter the facial vein and
thence to the jugular vein. The pathway of direction of flow is under sympathetic neural
control of the muscular coat of either vein which act as sphincters and redirect the flow along
one route or the other (21). The angularis occuli possesses alpha-adrenergic receptors
stimulation of which leads to venoconstriction whereas the receptors of the facial vein are
venodilator of the beta-adrenergic variety (21). Under generalized sympathetic stimulation
they are essentially antagonistic in their function. Blood entering the cranial cavernous sinuses
surrounds the arterial blood supply to the base of the brain which, in many panting species,
consists a network of vessels know as the carotid rete (6). Such an arrangement is an efficient
counter-current heat exchanger which allows the arterial supply to the brain to be cooled (2).
Although the existence of brain cooling has been demonstrated in many species that possess a
carotid rete there is no such structure in man, rabbit and horse. However, the internal carotid
artery of these species traverses the cranial cavernous sinus and there is a potential for countercurrent cooling although the absence of a vascular network such as the carotid rete would be
expected to minimize the efficacy of heat transfer. McConaghy et al (29) studied selective
brain cooling of the horse, a species which has no carotid rete and may not even be a panting
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animal. They clearly demonstrated the cooling of blood in the upper respiratory tract and
selective brain cooling during both heat exposure and exercise. Although man does not pant,
sweating from the head is particularly well developed and both cutaneous and respiratory
evaporative heat loss could contribute to selective brain cooling. Using tympanic membrane
temperature as an index of brain temperature and esophageal temperature as an index of
arterial temperature Cabanac & White (4) and White & Cabanac (39) have provided evidence
of selective brain cooling in man during both passive and exercise hyperthermia. The use of
tympanic membrane temperature as an index of brain temperature has been questioned until
some direct measurements of intracranial and subdural temperatures were made by Mariak and
colleagues on patients undergoing surgery for subarachnoid haemorrhage (27). They not only
confirmed the relationship between intracranial temperature and tympanic membrane
temperature (26) but also the link between upper respiratory cooling and selective brain
cooling (27).
They also concluded that, based on the speed of response to respiratory
evaporation, the transfer of heat from the nasal epithelium was by convective and not
conductive mechanisms.
The identification of selective brain cooling in both panting and nonpanting animals as well
as those species that do not possess a carotid rete was initially perceived as a mechanism for
the protection of a thermally vulnerable organ. However, this conclusion may be an
oversimplication and studies on free ranging animals demonstrate significant variability in the
extent to which it occurs and to quote from Jessen & Kuhnen (19) there is a “… need for
caution in assigning a specific function to the selective cooling mechanism.” However, it may
be possible in all the apparent contradictory conclusions to generate a possible working
hypothesis. The magnitude of selective brain cooling will depend on;
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1) the degree of nasal cooling and in this context the skin cooling by sweating in man may
contribute if cutaneous venous drainage is allowed to enter the angularis occuli vein,
2) distribution not only of cool venous blood to the cranial cavernous sinus but also the
routing of arterial blood to the heat exchangers,
3) the extent to which inhaled air is taken in through either the nose or mouth,
4) the role of selective brain cooling as a component of thermal homeostasis.
The work of Jessen and colleagues has been prominent in elucidating the thermal factors
that determine the initiation of selective brain cooling. The hypothalamic temperature sensors
themselves are cooled and selective brain cooling would, therefore, be part of a feedback loop
with brain temperature being the regulated variable. When the thermal affector systems are
partitioned into those in the brain or trunk Kuhnen & Jessen (23, 24) concluded that cranial
thermosensitivity largely determined the temperature threshold for selective brain cooling
whereas trunk temperatures influence the slope of the response above the threshold. Such a
control system integrates all the thermal inputs and dampens any oscillations in respiratory
evaporative heat loss.
The feedback loop for selective brain cooling will suppress panting. It has been proposed
that in dehydration the enhancement of panting and the use of selective brain cooling combined
with the suppression of sweating in goats (18, 32) can be viewed as a water retention
mechanism in that it will conserve approximately 35 % of the water intake (22). Brain cooling
thus becomes part of the cascade of water conservation responses to dehydration which are part
the hyperthermia of dehydration. The significance of open-mouthed panting and the
accompanying respiratory alkalosis which occurs during hyperthermia has been a mystery in
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terms of understanding its role in thermoregulation. The work of Aas-Hansen et al (1)
demonstrated that during open mouth panting in reindeer there is a redirection of inspired air
flow away from the nasal cavity to the mouth. Consequently there could be a reduced flow of
venous blood into the cranial cavernous sinus and a reduction in selective brain cooling.
Accordingly brain temperature rises and removes the inhibition of respiratory evaporative heat
loss, thereby assisting in total body heat dissipation.
In general the demonstration and replication of selective brain cooling is consistent under
laboratory conditions. However, non thermal factors such as the presence of an investigator
experimental area will suppress selective brain cooling (25).
Presumably these transient
periods of abandonment of selective brain cooling are mediated by a redirection of venous
blood flow away from the cavernous sinus. A similar event has been observed in studies of free
ranging animals where it is obvious that tight thermal control is not always apparent due to non
thermal factors. These may include the fright of being chased observed in wildebeest (20) or
bouts of spontaneous activity reported in free-ranging springbok (30). Exercise or generalized
sympathetic stimulation may therefore activate the alpha adrenergic receptors of the sphincter
muscle of the angularis occuli vein and divert flow into the facial vein and lead to a loss of
selective brain cooling.
Although there is evidence for selective brain cooling in man, recent observations on total
brain cooling during exercise with, or without hyperthermia (31) appear to negate the idea of
selective brain cooling. However, the general thesis of selective brain cooling has been that the
cooled area of the brain is confined to the thermosensitive regions of the hypothalamus and
generalized brain cooling may not take place.
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In summary, the evolution of research into respiratory and cutaneous evaporative heat loss
from the head and its relationship to selective brain cooling has moved away from the concept
of the brain as being uniquely vulnerable to hyperthermia to the notion that it represents part of
the control mechanism for thermal homeostasis.
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Figure Legend:
Figure 1. The distribution of the increasing respiratory minute volume into alveolar (x) and
dead space (•) ventilation during thermal tachypnea. Results from twelve experiments on
sheep. From (15) and used with permission from Blackwell Publishing.
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FIGURE 1
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